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The development and behavior of the free-living soil nematode, Caenorhabditis elegans, has been the subject of intensive study in recent years because of the advantages this simple metazoan offers for genetic, ultrastructural, and light microscopic analysis (reviewed by Riddle, 1978; Herman and Horvitz, 1980). This nematode develops by essentially invariant embryonic and post-embryonic cell lineages to produce an adult worm with fewer than 1000 somatic cells. The number and relative position of each of these cells with respect to one another is quite reproducible from animal to animal. Electron microscopy has proven to be a potent method for analysis of neural structure and development (White et al, 1978; Chalfie and Thomson, 1979; White et al, 1976); embryogenesis (Krieg et al, 1978), and the differentiation of specific tissues (Cox et al, 1981; Ward and Carrel, 1979).
Much of the fine structure of this nematode has been documented, including the anatomy of the neuro-muscular pharynx (Albertson and Thomson, 1976), the buccal capsule (Wright and Thomson, 1981), the anterior sensory anatomy (Ward et al, 1975; Ware et al, 1975), and the body wall musculature (Epstein et al, 1974; Waterston et al, 1980).
Our study of the genetic and environmental controls on postembryonic development in C. elegans (Albert et al, 1981; Swanson and Riddle, 1981) led us to investigate the anatomy of the secretory apparatus of this nematode in order to lay the groundwork for additional studies on the possible role of secretory-excretory activity in molting (Singh and Sulston, 1978) or in dauer larva formation (Riddle et al, 1981). The dauer (German: dauer = enduring) larva is a developmentally arrested stage which may be formed at the second larval molt in response to starvation or overcrowding. Dauer larvae survive exposure to detergents and other chemicals (Cassada and Russell, 1975), do not feed, and may survive for months until they encounter food, molt, and resume development. Neural integration of specific chemosensory cues, one of which is a Caenorhabditis-specific pheromone, apparently determines developmental fate (Golden and Riddle, 1982), but nothing is known about the endocrine mechanisms that may be employed to trigger morphogenesis of the dauer larva.
Caenorhabditis elegans contains only a few cells exhibiting glandular ultrastructure. Five such cells in the pharynx open into the lumen via short ducts (Albertson and Thomson, 1976). These cells may be innervated coordinately with pharyngeal muscles, suggesting that they may secrete digestive enzymes in concert with pharyngeal pumping. It has also been suggested that these glands may be involved in molting (Singh and Sulston, 1978). A gland outside the pharynx is associated with the excretory system. Although the general features of excretory gland structure have been determined by light microscopy (Sulston and Horvitz, 1977; Mounier, 1981), structure-function relationships for this gland and the associated excretory system have not been studied. The absence of documented ultrastructure for these cells represents a gap in our understanding of the biology of this animal.
Several studies of secretory anatomy have been done in parasitic nematode species (Rogers, 1968; Waddell, 1968; Lee, 1970; Narang, 1972; Romanowski et al, 1971; Davey and Hominick, 1973), but little is known about the physiology of these endocrine systems or the specific role they may play in development, reproduction, or behavior. Comparison of excretory systems among nematode species reveals that morphology is extremely variable. Some parasitic species apparently lack an excretory system altogether, at least during part of their life cycle (Chitwood and Chitwood, 1950). This variability suggests that the system has different functions in different species, and may be multifunctional in some. Osmoregulation is at least one function of the excretory cells in some species, because the rate of excretion is correlated with the osmotic strength of the medium (Weinstein, 1952; Croll et al., 1972). Although other possible functions such as waste-product clearance have not been rigorously established in any species, Ascarids have been shown to concentrate and expel injected dyes via the excretory duct (Behrenz, 1956). Because gland cells are associated with the excretory system in many species, it has been suggested that secreted products may be released to the outside environment through the excretory duct, or they may reach other internal tissues via the excretory canals (Romanowski et al., 1971). The excretory gland of the seal parasite, Phocanema decipiens, has been implicated in the release of peptidases involved in molting (Davey and Kan, 1968). Peptidases and esterases also have been identified in exsheathment fluid from other nematode species (Rogers, 1965). This paper describes the four cells found to be the structural components of the C. elegans secretory-excretory system. Cellular morphology has been reconstructed from electron micrographs of serially sectioned specimens. The nuclei of these cells are located in the head region on the ventral side of the pharynx, and on the ventral side of the intestine just posterior to the pha-ryngeal-intestinal valve. We have correlated changes in the physiology and developmental state of the nematode with changes in glandular morphology. In addition to the excretory gland, and duct cells previously described by light microscopic methods (Sulston and Horvitz, 1977; Mounier, 1981), we have characterized a specialized hypodermal cell, the "pore cell," which joins the excretory duct to the body-wall cuticle at the excretory pore. Also, we have characterized numerous subcellular morphological features which suggest specific physiological functions for each of the four cells. We have described a unique "secretory membrane" that joins the gland cell to the excretory system at the origin of the excretory duct. This membrane may selectively pass secreted products into the excretory duct or into the excretory sinus.
Adapted by Yusuf KARABEY for WORMATLAS, 2003